Seizure 23 (2014) 240–243
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Clinical letter
Encephalopathy with electrical status epilepticus during sleep: Cognitive and executive improvement after epilepsy surgery Concepcio´n Fournier-Del Castillo a,*, Marta Garcı´a-Ferna´ndez b, Marı´a-A´ngeles Pe´rez-Jime´nez b, Arturo Ugalde-Canitrot c, Juan A´lvarez-Linera d, Marı´a-Luz Ruiz-Falco´ e, Francisco Villarejo-Ortega f a
Neuropsychology Unit, Psychiatry and Clinical Psychology Section, Hospital Infantil Universitario Nin˜o Jesu´s, Avenida Mene´ndez Pelayo, 65, Madrid 28009, Spain b Epilepsy Monitoring Unit, Clinical Neurophysiology Section, Hospital Infantil Universitario Nin˜o Jesu´s, Avenida Mene´ndez Pelayo, 65, Madrid 28009, Spain c Epilepsy Monitoring Unit, Clinical Neurophysiology Service, Hospital Universitario La Paz, Paseo de la Castellana, 261, Madrid 28046, Spain d Neuroradiology Section, Diagnostic Imaging Service, Hospital Ruber Internacional, Calle de la Maso´, 38, Madrid 28034, Spain e Neurology Section, Hospital Infantil Universitario Nin˜o Jesu´s, Avenida Mene´ndez Pelayo, 65, Madrid 28009, Spain f Neurosurgery Service, Hospital Infantil Universitario Nin˜o Jesu´s, Avenida Mene´ndez Pelayo, 65, Madrid 28009, Spain
A R T I C L E I N F O
Article history: Received 17 April 2013 Received in revised form 30 August 2013 Accepted 1 September 2013
behavioural aspects. This study provides detailed information on neuropsychological function of two patients with ESES before and after treatment.
2. Case reports 2.1. Case 1 1. Introduction Electrical status epilepticus in sleep (ESES) is associated with neuropsychological disturbances, affecting cognitive and behavioural or socio-emotional domains. Attention deficit, impulsivity, lack of inhibition, difficulties in behavioural monitoring and regulation, diminished or scarcely modulated affective responses, apathy, poor social judgement, inadequate impulse control, impaired self-consciousness and poor interpersonal abilities, are indicators of executive dysfunction which variably express in children with ESES. Perinatal vascular and other congenital brain lesions coinvolving the thalamus are common aetiologies.1 Good response may be obtained with drugs, but ESES and progressive cognitive/ behavioural decline sometimes persist until the midteens and residual neuropsychological sequelae are common. Surgery is considered beneficial in patients with unilateral lesions, focal seizures and ESES. ESES resolution, seizure freedom, and improvements in development and behaviour have been described after resective surgery or callosotomy, but reported cases remain scarce,2,3 and little consideration is given to cognitive and
* Corresponding author. Tel.: +34 91 503 5900. E-mail address:
[email protected] (C. Fournier-Del Castillo).
Boy, born at 42 weeks gestational age by vaginal delivery, with meconial amniotic liquid. Apgar score: 6/7. He had neonatal convulsions, which were controlled. Neonatal MRI showed infarctions of both middle cerebral arteries (MCA) with a left predominance. At six months of age he developed a West syndrome, controlled with ACTH (Fig. 1). He remained seizure-free until the age of three years, when asymmetric tonic startle-related seizures began, with frequent falls. Various antiepileptic drugs (AED) were tried, obtaining only partial seizure control. Serial video-EEG studies showed occasional spike-waves over left frontal and occipital regions. No independent contralateral EEG discharges were recorded. Psychopedagogic control revealed good evolution except for expressive language, which was limited to a few poorly articulated words and the use of adapted signs and pictograms. Good adaptation to the environment was reported, as well as the absence of problematic behaviours. A control video-EEG performed when he was five years six months old showed ESES (spike frequency >85%). Six months later, after temporary electro-clinical improvement, seizures became daily and more intense. ESES was again documented and epilepsy surgery considered. As part of the pre-surgical work-up, a 3T-MRI performed at six years seven months of age showed porencephaly in the left MCA territory, involving the thalamus, and signs of a much milder previous infarction in the right MCA territory.
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Fig. 1. Case 1 graph indicating developmental quotient (DQ) evolution over time, pre-surgical MRI scan, pre- and post-surgical sleep EEG data (gain: 20 mV/mm), pre- and post-surgical executive (Behaviour Rating Inventory of Executive Function) and psychopathological (Achenbach Child Behaviour Checklist) profile graphs and post-surgical cognitive profile graph. In the executive, psychopathological and cognitive profile graphs, the thicker vertical lines mark the limit for significant disturbances, which deviate to the right.
Neuropsychological evaluation performed one month earlier showed severe attention disturbances, restlessness and inability to persist in tasks. Left functional hemispherectomy was performed at the age of six years eleven months. 2.1.1. Post-surgical outcome Seizure-freedom and resolution of ESES persist at latest followup (three years after surgery). Sporadic left occipital spikes during sleep remained, in all postsurgical controls. Noticeable improvements in executive functioning were documented three months after surgery, mostly in behavioural regulation aspects, emotional control and impulse inhibition (Table 1). Similarly, rule-breaking behaviour disappeared and attention problems minimized, but aggressive behaviour remained. Improvements in executive functions persist over time. A more extensive neuropsychological evaluation was performed one year after surgery. Tests requiring expressive language were not used due to persistent absence of speech. Normalization of behavioural regulation aspects of executive functioning and cognitive improvement allowed schooling continuation at a mainstream school.
2.2. Case 2 Boy, born after 37-week gestation by emergency caesarean section due to preeclampsia. Admitted for two weeks due to hypoglycaemia and low birth weight, with no apparent complications (Fig. 2). At the age of three months, a right hemiparesis was evident. MRI showed left hemispheric infarction. First seizure at the age of four years three months, described as eyes and mouth deviation to the right, with preserved consciousness, lasting 30 min. He had a second seizure eight months later with nausea, eyes and mouth deviation to the right, and vomiting. Similar events recurred every five or six months. Good cognitive and satisfactory socio-emotional evolutions without significant behavioural problems were reported initially. However, progressive attention decline, impulsivity and loss of acquired academic learning were noted at later follow-up. At the age of five years eleven months, EEG showed ESES. In the following months, progressive cognitive deterioration and a sleep disorder were reported. Various AEDs and steroids were tried without improvement. At the age of six years eight months he was referred to our hospital for surgical evaluation. Seizures remained sporadic.
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Table 1 Evolution of characteristic BRIEF (Gioia GA, Isquith PK, Guy SC, Kenworthy L. Behaviour Rating Inventory of Executive Function. USA: PAR Inc., 2000) and CBCL (Achenbach TM. Child Behavior Checklist. Burlington, VT: ASE-BA, University of Vermont; 2007) items that describe executive function disturbances, during ESES (encephalopathy with status epilepticus during sleep) and after surgery. Case 1
Case 2
Before surgery (during ESES)
3 months after surgery
Before surgery (during ESES)
3 months after surgery
Inhibitory control/impulsivity Acts too wild or out of control Quickly shifts from one activity to another Demands must be met immediately
Often Often Often
Never Never Sometimes
Often Often Sometimes
Never Never Sometimes
Shift Upset by new people or situations
Often
Never
Often
Never
Emotional control Has outbursts for little reason Sudden changes in mood or feeling
Often Often
Never Never
Never Sometimes
Never Never
Repetitive behaviours Repeatedly rocks head or body
Never
Never
Often
Never
Relational-social Shows little interest in things around him Does not seem to feel guilty after misbehaving Punishment does not change his behaviour
Sometimes Often Often
Never Never Sometimes
Often Often Often
Never Never Never
Attention Daydreams or gets lost in thoughts Cannot concentrate, cannot pay attention for long
Often Often
Sometimes Sometimes
Often Often
Never Sometimes
Self-monitoring/interpersonal awareness Is unaware of how his behaviour affects or bothers others Does not notice when his behaviour causes negative reactions
Often Often
Never Never
Often Often
Never Never
Fig. 2. Case 2 graph indicating developmental quotient (DQ) evolution over time, pre-surgical MRI scan, pre- and post-surgical sleep EEG data (gain: 20 mV/mm), pre- and post-surgical executive (Behaviour Rating Inventory of Executive Function) and psychopathological (Achenbach Child Behaviour Checklist) profile graphs and post-surgical cognitive profile graph. In the executive, psychopathological and cognitive profile graphs, the thicker vertical lines mark the limit for significant disturbances, which deviate to the right.
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Video-EEG showed frequent asynchronous spike-waves over left parieto-occipital and central regions, appearing as generalized discharges during sleep, involving over 85% of NREM. 3T-MRI showed a left destructive pattern (MCA territory, involving the thalamus). Neuropsychological evaluation performed at the age of six years eight months showed erratic, unpredictable and agitated behaviour, inability to sustain attention, scarce ocular contact, absence of response to verbal commands, and frequent stereotyped behaviours (body rocking and hand flapping). Language was limited to echolalic productions. Left functional hemispherectomy was performed at the age of six years ten months.
surgery must be considered even in the absence of clinical seizures. Surgery was highly effective in both our cases. Significantly improved cognitive level after surgery (catch-up development) has been referred to be possible, although rare, in children with ESES.2,3 This was documented in our case 1, despite having bilateral injury. In case 2, general cognitive scores (DQ/IQ) stabilized, reflecting a halt to deterioration. Furthermore, as in previously reported cases,4 ESES resolution significantly improved self-control/inhibition and socio-emotional behaviour favouring adaptation to environmental demands. We found marked improvements in neuropsychological function in patients with ESES after surgery.
2.2.1. Post-surgical outcome Seizure-freedom and resolution of ESES persist, two years after surgery. Occasional spikes limited to the left frontal region remained, in all postsurgical controls. Executive functioning normalized already at three months after surgery (Table 1) and improvements persist over time. Further neuropsychological evaluation performed one year after surgery showed that deterioration stopped. Behavioural and executive improvements have allowed schooling at a mainstream school with psychopedagogic supports.
Conflict of interest statement
3. Discussion In children with refractory ESES, unilateral lesions, and neuropsychological disturbances related to EEG activity, epilepsy
We declare that we have no conflict of interest. References 1. Sa´nchez Ferna´ndez I, Takeoka M, Tas E, Peters JM, Prabhu SP, Stannard KM, et al. Early thalamic lesions in patients with sleep-potentiated epileptiform activity. Neurology 2012;78:1721–7. 2. Loddenkemper T, Cosmo G, Kotagal P, Haut J, Klass P, Gupta A, et al. Epilepsy surgery in children with electrical status epilepticus in sleep. Neurosurgery 2009;64:328–37. 3. Peltola ME, Liukkonen E, Granstro¨m ML, Paetau R, Kantola-Sorsa E, Valanne L, et al. The effect of surgery in encephalopathy with electrical status epilepticus during sleep. Epilepsia 2011;52:602–9. 4. Veggiotti P, Bova S, Granocchio E, Papalia G, Termine C, Lanzi G. Acquired epileptic frontal syndrome as long-term outcome in two children with CSWS. Neurophysiol Clin 2001;31:387–97.